Meconium microbiota types dominated by lactic acid or enteric bacteria are differentially associated with maternal eczema and respiratory problems in infants

Clinical and Experimental Allergy

Volumn 43, Issue 2, 2013, Pages 198-211

  Gosalbes, M J ^a,b   Llop, S ^b,c   Valles Y ^a   Moya, A ^a,b   Ballester, F ^b,c,d   Francino, M P ^e  

^a UNIVERSITY OF VALENCIA   (Spain)

^b CIBER EPIDEMIOLOGÍA Y SALUD PÚBLICA CIBERESP   (Spain)

^c Centro Superior de Investigacion en Salud Publica   (Spain)

^d UNIVERSITY OF VALENCIA   (Spain)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

16S rRNA; Atopy; Eczema; Gastrointestinal tract; Pyrosequencing

Indexed keywords

RNA 16S;

ADULT; ARTICLE; ASTHMA; ATOPIC DERMATITIS; BACTERIAL FLORA; BACTEROIDES; BRONCHITIS; CHRYSEOBACTERIUM; CLINICAL ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; ECZEMA; ENTEROCOCCACEAE; ENTEROCOCCUS; ESCHERICHIA; FECES MICROFLORA; FEMALE; GASTROINTESTINAL TRACT; HUMAN; INTESTINE FLORA; LACTIC ACID BACTERIUM; LACTOCOCCUS; LEUCONOSTOC; LEUCONOSTOCACEAE; LIFESTYLE; MECONIUM; MECONIUM ASPIRATION; MEDICAL HISTORY; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PYROSEQUENCING; RESPIRATORY TRACT DISEASE; RHINITIS; SHIGELLA; SKIN FLORA; STAPHYLOCOCCUS; STREPTOCOCCACEAE; STREPTOCOCCUS; VAGINA FLORA; WHEEZING;

ADULT; DNA, BACTERIAL; ECZEMA; ENTEROBACTERIACEAE; FEMALE; HUMANS; HYPERSENSITIVITY, IMMEDIATE; INFANT, NEWBORN; INTESTINES; LACTOBACILLALES; LIFE STYLE; MECONIUM; METAGENOME; PHYLOGENY; PREGNANCY; RISK FACTORS; RNA, RIBOSOMAL, 16S;

EID: 84872506745     PISSN: 09547894     EISSN: 13652222     Source Type: Journal    
DOI: 10.1111/cea.12063     Document Type: Article

References (75)

1. DiGiulio DB, Romero R, Amogan HP etal. Microbial prevalence, diversity and abundance in amniotic fluid during preterm labor: a molecular and culture-based investigation. PLoS ONE 2008; 3:e3056.
2. Jiménez E, Fernandez L, Marín ML etal. Isolation of commensal bacteria from umbilical cord blood of healthy neonates born by cesarean section. Curr Microbiol 2005; 51:270-4.
3. Jiménez E, Marín ML, Martín R etal. Is meconium from healthy newborns actually sterile? Res Microbiol 2008; 159:187-93.
4. Mshvildadze M, Neu J, Shuster J, Theriaque D, Li N, Mai V. Intestinal microbial ecology in premature infants assessed with non-culture-based techniques. J Pediatr 2010; 156:20-5.
5. Madan JC, Salari RC, Saxena D etal. Gut microbial colonisation in premature neonates predicts neonatal sepsis. Arch Dis Child Fetal Neonatal Ed 2012; 97:F456-62.
6. Vallès Y, Gosalbes MJ, de Vries LE, Abellán JJ, Francino MP. Metagenomics and development of the gut microbiota in infants. Clin Microbiol Infect 2012; 18 (Suppl. 4):21-6.
7. Rescigno M, Rotta G, Valzasina B, Ricciardi-Castagnoli P. Dendritic cells shuttle microbes across gut epithelial monolayers. Immunobiology 2001; 204:572-81.
8. Perez PF, Dore J, Leclerc M etal. Bacterial imprinting of the neonatal immune system: lessons from maternal cells? Pediatrics 2007; 119:e724-32.
9. Bjorksten B. Environment and infant immunity. Proc Nutr Soc 1999; 58:729-32.
10. Penders J, Thijs C, van den Brandt PA etal. Gut microbiota composition and development of atopic manifestations in infancy: the KOALA Birth Cohort Study. Gut 2007; 56:661-7.
11. Wold AE. The hygiene hypothesis revised: is the rising frequency of allergy due to changes in the intestinal flora? Allergy 1998; 53:20-5.
12. Bjorksten B, Sepp E, Julge K, Voor T, Mikelsaar M. Allergy development and the intestinal microflora during the first year of life. J Allergy Clin Immunol 2001; 108:516-20.
13. Kalliomaki M, Kirjavainen P, Eerola E, Kero P, Salminen S, Isolauri E. Distinct patterns of neonatal gut microflora in infants in whom atopy was and was not developing. J Allergy Clin Immunol 2001; 107:129-34.
14. Sjogren YM, Jenmalm MC, Bottcher MF, Bjorksten B, Sverremark-Ekstrom E. Altered early infant gut microbiota in children developing allergy up to 5years of age. Clin Exp Allergy 2009; 39:518-26.
15. Penders J, Stobberingh EE, Thijs C etal. Molecular fingerprinting of the intestinal microbiota of infants in whom atopic eczema was or was not developing. Clin Exp Allergy 2006; 36:1602-8.
16. Wang M, Karlsson C, Olsson C etal. Reduced diversity in the early fecal microbiota of infants with atopic eczema. J Allergy Clin Immunol 2008; 121:129-34.
17. Sjogren YM, Tomicic S, Lundberg A etal. Influence of early gut microbiota on the maturation of childhood mucosal and systemic immune responses. Clin Exp Allergy 2009; 39:1842-51.
18. Bisgaard H, Li N, Bonnelykke K etal. Reduced diversity of the intestinal microbiota during infancy is associated with increased risk of allergic disease at school age. J Allergy Clin Immunol 2011; 128:646-52.
19. Abrahamsson TR, Jakobsson HE, Andersson AF, Bjorksten B, Engstrand L, Jenmalm MC. Low diversity of the gut microbiota in infants with atopic eczema. J Allergy Clin Immunol 2012; 129:434-40. 440 e431-432.
20. Sepp E, Julge K, Mikelsaar M, Bjorksten B. Intestinal microbiota and immunoglobulin E responses in 5-year-old Estonian children. Clin Exp Allergy 2005; 35:1141-6.
21. Sepp E, Julge K, Vasar M, Naaber P, Bjorksten B, Mikelsaar M. Intestinal microflora of Estonian and Swedish infants. Acta Paediatr 1997; 86:956-61.
22. Mah KW, Bjorksten B, Lee BW etal. Distinct pattern of commensal gut microbiota in toddlers with eczema. Int Arch Allergy Immunol 2006; 140:157-63.
23. Murray CS, Tannock GW, Simon MA etal. Fecal microbiota in sensitized wheezy and non-sensitized non-wheezy children: a nested case-control study. Clin Exp Allergy 2005; 35:741-5.
24. Hong WS, Chen YP, Chen MJ. The antiallergic effect of kefir Lactobacilli. J Food Sci 2010; 75:H244-53.
25. Watanabe S, Narisawa Y, Arase S etal. Differences in fecal microflora between patients with atopic dermatitis and healthy control subjects. J Allergy Clin Immunol 2003; 111:587-91.
26. Ribas-Fitó N, Ramón R, Ballester F etal. Child health and the environment: the INMA Spanish Study. Paediatr Perinat Epidemiol 2006; 20:403-10.
27. Cole JR, Wang Q, Cardenas E etal. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 2009; 37:D141-5.
28. Chao A. Nonparametric estimation of the number of classes in a population. Scand J Stat 1984; 11:256-70.
29. Shannon CE. A mathematical theory of communication. Bell Syst Tech J 1948; 27:379-656.
30. Oksanen J. VEGAN, a package of R functions for community ecology. J Veg Sci 2003; 14:927-30.
31. Team-RDC. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing, 2010.
32. Hamady M, Lozupone C, Knight R. Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J 2010; 4:17-27.
33. Domínguez-Bello MG, Costello EK, Contreras M etal. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci U S A 2010; 107:11971-5.
34. Li W, Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 2006; 22:1658-9.
35. Schloss PD, Westcott SL, Ryabin T etal. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 2009; 75:7537-41.
36. DeSantis TZ, Hugenholtz P, Larsen N etal. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 2006; 72:5069-72.
37. Price MN, Dehal PS, Arkin AP. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 2009; 26:1641-50.
38. Hanifin JM, Rajka G. Diagnostic features of atopic dermatitis. Acta Derm Venereol (Stockh) 1980; 92(Suppl):44-7.
39. Martorell Aragonés A, Febrer Bosch MI. Attitude towards the child affected by atopic dermatitis. In: Garde J, ed. Protocolos de inmunología clínica y alergología. Madrid, Spain: Asociación Española de Pediatría (AEP) y Sociedad Española de Inmunología Clínica y Alergia Pediátrica (SEICAP), 2003:23-32.
40. Martorell Aragones A, Felix Toledo R, Martorell Calatayud A, Cerda Mir JC. Epidemiologic, clinical and socioeconomic factors of atopic dermatitis in Spain: Alergologica-2005. J Investig Allergol Clin Immunol 2009; 19(Suppl 2):27-33.
41. Aagaard K, Riehle K, Ma J etal. A metagenomic approach to characterization of the vaginal microbiome signature in pregnancy. PLoS ONE 2012; 7:e36466.
42. Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R. Bacterial community variation in human body habitats across space and time. Science 2009; 326:1694-7.
43. Cabrera-Rubio R, Collado MC, Laitinen K, Salminen S, Isolauri E, Mira A. The human milk microbiome changes over lactation and is shaped by maternal weight and mode of delivery. Am J Clin Nutr 2012; 96:544-51.
44. Finke D, Kraehenbuhl JP. Formation of Peyer's patches. Curr Opin Genet Dev 2001; 11:561-7.
45. Gunther U, Holloway JA, Gordon JN etal. Phenotypic characterization of CD3-7+ cells in developing human intestine and an analysis of their ability to differentiate into T cells. J Immunol 2005; 174:5414-22.
46. Blumer N, Pfefferle PI, Renz H. Development of mucosal immune function in the intrauterine and early postnatal environment. Curr Opin Gastroenterol 2007; 23:655-60.
47. Jones CA, Vance GH, Power LL, Pender SL, Macdonald TT, Warner JO. Costimulatory molecules in the developing human gastrointestinal tract: a pathway for fetal allergen priming. J Allergy Clin Immunol 2001; 108:235-41.
48. Amoudruz P, Holmlund U, Malmstrom V etal. Neonatal immune responses to microbial stimuli: is there an influence of maternal allergy? J Allergy Clin Immunol 2005; 115:1304-10.
49. Schaub B, Campo M, He H etal. Neonatal immune responses to TLR2 stimulation: influence of maternal atopy on Foxp3 and IL-10 expression. Respir Res 2006; 7:40.
50. Reece P, Thanendran A, Crawford L etal. Maternal allergy modulates cord blood hematopoietic progenitor Toll-like receptor expression and function. J Allergy Clin Immunol 2011; 127:447-53.
51. Schaub B, Liu J, Hoppler S etal. Impairment of T-regulatory cells in cord blood of atopic mothers. J Allergy Clin Immunol 2008; 121:1491-9, 1499 e1491-1413.
52. Johnson CC, Ownby DR, Peterson EL. Parental history of atopic disease and concentration of cord blood IgE. Clin Exp Allergy 1996; 26:624-9.
53. Magnusson CG. Maternal smoking influences cord serum IgE and IgD levels and increases the risk for subsequent infant allergy. J Allergy Clin Immunol 1986; 78:898-904.
54. Devereux G, Barker RN, Seaton A. Antenatal determinants of neonatal immune responses to allergens. Clin Exp Allergy 2002; 32:43-50.
55. Noakes PS, Hale J, Thomas R, Lane C, Devadason SG, Prescott SL. Maternal smoking is associated with impaired neonatal toll-like-receptor-mediated immune responses. Eur Respir J 2006; 28:721-9.
56. Prescott SL. Effects of early cigarette smoke exposure on early immune development and respiratory disease. Paediatr Respir Rev 2008; 9:3-9; quiz 10.
57. Abelius MS, Ernerudh J, Berg G, Matthiesen L, Nilsson LJ, Jenmalm MC. High cord blood levels of the T-helper 2-associated chemokines CCL17 and CCL22 precede allergy development during the first 6years of life. Pediatr Res 2011; 70:495-500.
58. Abrahamsson TR, Sandberg Abelius M, Forsberg A, Bjorksten B, Jenmalm MC. A Th1/Th2-associated chemokine imbalance during infancy in children developing eczema, wheeze and sensitization. Clin Exp Allergy 2011; 41:1729-39.
59. Miyahara H, Okazaki N, Nagakura T, Korematsu S, Izumi T. Elevated umbilical cord serum TARC/CCL17 levels predict the development of atopic dermatitis in infancy. Clin Exp Allergy 2011; 41:186-91.
60. Halonen M, Stern D, Taussig LM, Wright A, Ray CG, Martinez FD. The predictive relationship between serum IgE levels at birth and subsequent incidences of lower respiratory illnesses and eczema in infants. Am Rev Respir Dis 1992; 146:866-70.
61. Huurre A, Laitinen K, Rautava S, Korkeamaki M, Isolauri E. Impact of maternal atopy and probiotic supplementation during pregnancy on infant sensitization: a double-blind placebo-controlled study. Clin Exp Allergy 2008; 38:1342-8.
62. Kjellman NI. Effect of parental smoking on IgE levels in children. Lancet 1981; 1:993-4.
63. Ege MJ, Bieli C, Frei R etal. Prenatal farm exposure is related to the expression of receptors of the innate immunity and to atopic sensitization in school-age children. J Allergy Clin Immunol 2006; 117:817-23.
64. Schaub B, Liu J, Hoppler S etal. Maternal farm exposure modulates neonatal immune mechanisms through regulatory T cells. J Allergy Clin Immunol 2009; 123:774-82. e775.
65. Carbonaro M, Mattera M. Polyphenoloxidase activity and polyphenol levels in organically and conventionally grown peach (Prunus persicaI L., cv. Regina bianca) and pear (Pyrus communis L., cv. Williams). Food Chem 2001; 72:419-24.
66. Dani C, Oliboni LS, Vanderlinde R, Bonatto D, Salvador M, Henriques JA. Phenolic content and antioxidant activities of white and purple juices manufactured with organically- or conventionally-produced grapes. Food Chem Toxicol 2007; 45:2574-80.
67. Mitchell AE, Hong YJ, Koh E etal. Ten-year comparison of the influence of organic and conventional crop management practices on the content of flavonoids in tomatoes. J Agric Food Chem 2007; 55:6154-9.
68. Murata Y, Amao M, Yoneda J, Hamuro J. Intracellular thiol redox status of macrophages directs the Th1 skewing in thioredoxin transgenic mice during aging. Mol Immunol 2002; 38:747-57.
69. Utsugi M, Dobashi K, Ishizuka T etal. c-Jun N-terminal kinase negatively regulates lipopolysaccharide-induced IL-12 production in human macrophages: role of mitogen-activated protein kinase in glutathione redox regulation of IL-12 production. J Immunol 2003; 171:628-35.
70. Wu T, Chellemi DO, Graham JH, Martin KJ, Rosskopf EN. Comparison of soil bacterial communities under diverse agricultural land management and crop production practices. Microb Ecol 2008; 55:293-310.
71. Reeve JR, Schadt CW, Carpenter-Boggs L, Kang S, Zhou J, Reganold JP. Effects of soil type and farm management on soil ecological functional genes and microbial activities. ISME J 2010; 4:1099-107.
72. Ottesen AR, White JR, Skaltsas DN, Newell MJ, Walsh CS. Impact of organic and conventional management on the phyllosphere microbial ecology of an apple crop. J Food Prot 2009; 72:2321-5.
73. Wise MG, Siragusa GR. Quantitative analysis of the intestinal bacterial community in one- to three-week-old commercially reared broiler chickens fed conventional or antibiotic-free vegetable-based diets. J Appl Microbiol 2007; 102:1138-49.
74. van de Kant KD, Klaassen EM, Jobsis Q, Nijhuis AJ, van Schayck OC, Dompeling E. Early diagnosis of asthma in young children by using non-invasive biomarkers of airway inflammation and early lung function measurements: study protocol of a case-control study. BMC Public Health 2009; 9:210.
75. Bezirtzoglou E, Tsiotsias A, Welling GW. Microbiota profile in feces of breast- and formula-fed newborns by using fluorescence in situ hybridization (FISH). Anaerobe 2011; 17:478-82.